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ORIGINAL RESEARCH

SK-Channel Activation Alters Peripheral Metabolic Pathways in Mice, but Not Lipopolysaccharide-Induced Fever or Inflammation

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Pages 509-531 | Published online: 23 Jan 2022

References

  • Schneiders J, Fuchs F, Damm J, et al. The transcription factor nuclear factor interleukin 6 mediates pro- and anti-inflammatory responses during LPS-induced systemic inflammation in mice. Brain Behav Immun. 2015;48:147–164. doi:10.1016/j.bbi.2015.03.008
  • Dantzer R, O’Connor JC, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci. 2008;9(1):46–56. doi:10.1038/nrn2297
  • Rummel C. Inflammatory transcription factors as activation markers and functional readouts in immune-to-brain communication. Brain Behav Immun. 2016;54:1–14. doi:10.1016/j.bbi.2015.09.003
  • Peek V, Harden LM, Damm J, et al. LPS primes brain responsiveness to high mobility group box-1 protein. Pharmaceuticals. 2021;14(6). doi:10.3390/ph14060558.
  • Cartmell T, Poole S, Turnbull AV, Rothwell NJ, Luheshi GN. Circulating interleukin-6 mediates the febrile response to localised inflammation in rats. J Physiol. 2000;526(Pt 3):653–661. doi:10.1111/j.1469-7793.2000.00653.x
  • LeMay LG, Vander AJ, Kluger MJ. Role of interleukin 6 in fever in rats. Am J Physiol. 1990;258(3 Pt 2):R798–803. doi:10.1152/ajpregu.1990.258.3.R798
  • Rummel C, Voss T, Matsumura K, et al. Nuclear STAT3 translocation in Guinea pig and rat brain endothelium during systemic challenge with lipopolysaccharide and interleukin-6. J Comp Neurol. 2005;491(1):1–14. doi:10.1002/cne.20653
  • Rummel C, Hubschle T, Gerstberger R, Roth J. Nuclear translocation of the transcription factor STAT3 in the Guinea pig brain during systemic or localized inflammation. J Physiol. 2004;557(Pt 2):671–687. doi:10.1113/jphysiol.2003.058834
  • Laflamme N, Rivest S. Effects of systemic immunogenic insults and circulating proinflammatory cytokines on the transcription of the inhibitory factor kappaB alpha within specific cellular populations of the rat brain. J Neurochem. 1999;73(1):309–321. doi:10.1046/j.1471-4159.1999.0730309.x
  • Benarroch EE. Microglia: multiple roles in surveillance, circuit shaping, and response to injury. Neurology. 2013;81(12):1079–1088. doi:10.1212/WNL.0b013e3182a4a577
  • Chan WY, Kohsaka S, Rezaie P. The origin and cell lineage of microglia: new concepts. Brain Res Rev. 2007;53(2):344–354. doi:10.1016/j.brainresrev.2006.11.002
  • Berve K, West BL, Martini R, Groh J. Sex- and region-biased depletion of microglia/macrophages attenuates CLN1 disease in mice. J Neuroinflammation. 2020;17(1):323. doi:10.1186/s12974-020-01996-x
  • Masuch A, van der Pijl R, Funer L, et al. Microglia replenished OHSC: a culture system to study in vivo like adult microglia. Glia. 2016;64(8):1285–1297. doi:10.1002/glia.23002
  • Valdearcos M, Robblee MM, Benjamin DI, Nomura DK, Xu AW, Koliwad SK. Microglia dictate the impact of saturated fat consumption on hypothalamic inflammation and neuronal function. Cell Rep. 2014;9(6):2124–2138. doi:10.1016/j.celrep.2014.11.018
  • Nissen JC, Thompson KK, West BL, Tsirka SE. Csf1R inhibition attenuates experimental autoimmune encephalomyelitis and promotes recovery. Exp Neurol. 2018;307:24–36. doi:10.1016/j.expneurol.2018.05.021
  • Teeling JL, Perry VH. Systemic infection and inflammation in acute CNS injury and chronic neurodegeneration: underlying mechanisms. Neuroscience. 2009;158(3):1062–1073. doi:10.1016/j.neuroscience.2008.07.031
  • Hoffmann A, Kann O, Ohlemeyer C, Hanisch UK, Kettenmann H. Elevation of basal intracellular calcium as a central element in the activation of brain macrophages (microglia): suppression of receptor-evoked calcium signaling and control of release function. J Neurosci. 2003;23(11):4410–4419. doi:10.1523/JNEUROSCI.23-11-04410.2003
  • Wuchert F, Ott D, Murgott J, et al. Rat area postrema microglial cells act as sensors for the toll-like receptor-4 agonist lipopolysaccharide. J Neuroimmunol. 2008;204(1–2):66–74. doi:10.1016/j.jneuroim.2008.07.017
  • Bauer J, Sminia T, Wouterlood FG, Dijkstra CD. Phagocytic activity of macrophages and microglial cells during the course of acute and chronic relapsing experimental autoimmune encephalomyelitis. J Neurosci Res. 1994;38(4):365–375. doi:10.1002/jnr.490380402
  • Damoiseaux JG, Dopp EA, Calame W, Chao D, MacPherson GG, Dijkstra CD. Rat macrophage lysosomal membrane antigen recognized by monoclonal antibody ED1. Immunology. 1994;83(1):140–147.
  • Goings GE, Kozlowski DA, Szele FG. Differential activation of microglia in neurogenic versus non-neurogenic regions of the forebrain. Glia. 2006;54(4):329–342. doi:10.1002/glia.20381
  • Monje ML, Toda H, Palmer TD. Inflammatory blockade restores adult hippocampal neurogenesis. Science. 2003;302(5651):1760–1765. doi:10.1126/science.1088417
  • Srinivasan K, Friedman BA, Larson JL, et al. Untangling the brain’s neuroinflammatory and neurodegenerative transcriptional responses. Nat Commun. 2016;7:11295. doi:10.1038/ncomms11295
  • Stocker M, Pedarzani P. Differential distribution of three Ca(2+)-activated K(+) channel subunits, SK1, SK2, and SK3, in the adult rat central nervous system. Mol Cell Neurosci. 2000;15(5):476–493. doi:10.1006/mcne.2000.0842
  • Sailer CA, Kaufmann WA, Marksteiner J, Knaus HG. Comparative immunohistochemical distribution of three small-conductance Ca2+-activated potassium channel subunits, SK1, SK2, and SK3 in mouse brain. Mol Cell Neurosci. 2004;26(3):458–469. doi:10.1016/j.mcn.2004.03.002
  • Kuiper EFE, Nelemans A, Luiten P, Nijholt I, Dolga A, Eisel U. KCa2 and KCa3 Channels in Learning and Memory Processes, and Neurodegeneration. Front Pharmacol. 2012;3. doi:10.3389/fphar.2012.00003
  • Allen D, Nakayama S, Kuroiwa M, et al. SK2 channels are neuroprotective for ischemia-induced neuronal cell death. J Cereb Blood Flow Metab. 2011;31(12):2302–2312. doi:10.1038/jcbfm.2011.90
  • Dolga AM, Granic I, Blank T, et al. TNF-α mediates neuroprotection against glutamate-induced excitotoxicity via NF-κB-dependent up-regulation of KCa2.2 channels. J Neurochem. 2008. doi:10.1111/j.1471-4159.2008.05701.x
  • Dolga AM, Terpolilli N, Kepura F, et al. KCa2 channels activation prevents [Ca2+]i deregulation and reduces neuronal death following glutamate toxicity and cerebral ischemia. Cell Death Dis. 2011;2(4):e147. doi:10.1038/cddis.2011.30
  • Krabbendam IE, Honrath B, Dilberger B, et al. SK channel-mediated metabolic escape to glycolysis inhibits ferroptosis and supports stress resistance in C. elegans. Cell Death Dis. 2020;11(4):263. doi:10.1038/s41419-020-2458-4
  • Honrath B, Matschke L, Meyer T, et al. SK2 channels regulate mitochondrial respiration and mitochondrial Ca(2+) uptake. Cell Death Differ. 2017;24(5):761–773. doi:10.1038/cdd.2017.2
  • Dolga AM, Letsche T, Gold M, et al. Activation of KCNN3/SK3/K(Ca)2.3 channels attenuates enhanced calcium influx and inflammatory cytokine production in activated microglia. Glia. 2012;60(12):2050–2064. doi:10.1002/glia.22419
  • Hougaard C, Eriksen BL, Jørgensen S, et al. Selective positive modulation of the SK3 and SK2 subtypes of small conductance Ca2+-activated K+channels. Br J Pharmacol. 2007;151(5):655–665. doi:10.1038/sj.bjp.0707281
  • Khanna R, Roy L, Zhu X, Schlichter LC. K+ channels and the microglial respiratory burst. Am J Physiol Cell Physiol. 2001;280(4):C796–806. doi:10.1152/ajpcell.2001.280.4.C796
  • Schlichter LC, Kaushal V, Moxon-Emre I, Sivagnanam V, Vincent C. The Ca2+ activated SK3 channel is expressed in microglia in the rat striatum and contributes to microglia-mediated neurotoxicity in vitro. J Neuroinflammation. 2010;7(1):4. doi:10.1186/1742-2094-7-4
  • Dolga AM, Culmsee C. Protective Roles for Potassium SK/K(Ca)2 Channels in Microglia and Neurons. Front Pharmacol. 2012;3:196. doi:10.3389/fphar.2012.00196
  • Damm J, Luheshi GN, Gerstberger R, Roth J, Rummel C. Spatiotemporal nuclear factor interleukin-6 expression in the rat brain during lipopolysaccharide-induced fever is linked to sustained hypothalamic inflammatory target gene induction. J Comp Neurol. 2011;519(3):480–505. doi:10.1002/cne.22529
  • Gautron L, Lafon P, Chaigniau M, Tramu G, Laye S. Spatiotemporal analysis of signal transducer and activator of transcription 3 activation in rat brain astrocytes and pituitary following peripheral immune challenge. Neuroscience. 2002;112(3):717–729. doi:10.1016/S0306-4522(02)00115-X
  • Aguilar-Valles A, Kim J, Jung S, Woodside B, Luheshi GN. Role of brain transmigrating neutrophils in depression-like behavior during systemic infection. Mol Psychiatry. 2014;19(5):599–606. doi:10.1038/mp.2013.137
  • Roth J, Blatteis CM. Mechanisms of fever production and lysis: lessons from experimental LPS fever. Compr Physiol. 2014;4(4):1563–1604.
  • Bredehoft J, Bhandari DR, Pflieger FJ, et al. Visualizing and Profiling Lipids in the OVLT of Fat-1 and Wild Type Mouse Brains during LPS-Induced Systemic Inflammation Using AP-SMALDI MSI. ACS Chem Neurosci. 2019;10(10):4394–4406. doi:10.1021/acschemneuro.9b00435
  • Roth J, Harre EM, Rummel C, Gerstberger R, Hubschle T. Signaling the brain in systemic inflammation: role of sensory circumventricular organs. Front Biosci. 2004;9:290–300. doi:10.2741/1241
  • Chen MX, Gorman SA, Benson B, et al. Small and intermediate conductance Ca(2+)-activated K+ channels confer distinctive patterns of distribution in human tissues and differential cellular localisation in the colon and corpus cavernosum. Naunyn Schmiedebergs Arch Pharmacol. 2004;369(6):602–615. doi:10.1007/s00210-004-0934-5
  • Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84(1):277–359. doi:10.1152/physrev.00015.2003
  • Mourre C, Manrique C, Camon J, et al. Changes in SK channel expression in the basal ganglia after partial nigrostriatal dopamine lesions in rats: functional consequences. Neuropharmacology. 2017;113(Pt A):519–532. doi:10.1016/j.neuropharm.2016.11.003
  • Wollweber BT, Schneider H, Voigt K. Ethanol effects on temperature-sensitive hypothalamic neurons in rat brain slices. J Therm Biol. 2004;29:345–350. doi:10.1016/j.jtherbio.2004.08.083
  • Herrik KF, Redrobe JP, Holst D, et al. CyPPA, a Positive SK3/SK2 Modulator, Reduces Activity of Dopaminergic Neurons, Inhibits Dopamine Release, and Counteracts Hyperdopaminergic Behaviors Induced by Methylphenidate1. Front Pharmacol. 2012;3:3.
  • Paxinos G, Franklin KBJ. The Mouse Brain in Stereotaxic Coordinates. San Diego, California, USA: Academic Press; 2001.
  • Simm B, Ott D, Pollatzek E, et al. Effects of prostaglandin E2 on cells cultured from the rat organum vasculosum laminae terminalis and median preoptic nucleus. Neuroscience. 2016;313:23–35. doi:10.1016/j.neuroscience.2015.11.034
  • Lorke DE, Ip CW, Schumacher U. Increased number of microglia in the brain of severe combined immunodeficient (SCID) mice. Histochem Cell Biol. 2008;130(4):693–697. doi:10.1007/s00418-008-0463-2
  • Rummel C, Sachot C, Poole S, Luheshi GN. Circulating interleukin-6 induces fever through a STAT3-linked activation of COX-2 in the brain. Am J Physiol Regul Integr Comp Physiol. 2006;291(5):R1316–1326. doi:10.1152/ajpregu.00301.2006
  • Rummel C, Inoue W, Sachot C, Poole S, Hubschle T, Luheshi GN. Selective contribution of interleukin-6 and leptin to brain inflammatory signals induced by systemic LPS injection in mice. J Comp Neurol. 2008;511(3):373–395. doi:10.1002/cne.21850
  • Torika N, Asraf K, Apte RN, Fleisher-Berkovich S. Candesartan ameliorates brain inflammation associated with Alzheimer’s disease. CNS Neurosci Ther. 2018;24(3):231–242. doi:10.1111/cns.12802
  • Latta CH, Sudduth TL, Weekman EM, et al. Determining the role of IL-4 induced neuroinflammation in microglial activity and amyloid-β using BV2 microglial cells and APP/PS1 transgenic mice. J Neuroinflammation. 2015;12(1):41. doi:10.1186/s12974-015-0243-6
  • Perego C, Fumagalli S, De Simoni M-G. Temporal pattern of expression and colocalization of microglia/macrophage phenotype markers following brain ischemic injury in mice. J Neuroinflammation. 2011;8(1):174. doi:10.1186/1742-2094-8-174
  • Hovens IB, Nyakas C, Schoemaker RG. A novel method for evaluating microglial activation using ionized calcium-binding adaptor protein-1 staining: cell body to cell size ratio. Neuroimmunol Neuroinflammation. 2014;1(2):82–88. doi:10.4103/2347-8659.139719
  • Damm J, Harden LM, Gerstberger R, Roth J, Rummel C. The putative JAK-STAT inhibitor AG490 exacerbates LPS-fever, reduces sickness behavior, and alters the expression of pro- and anti-inflammatory genes in the rat brain. Neuropharmacology. 2013;71:98–111. doi:10.1016/j.neuropharm.2013.03.014
  • Dangarembizi R, Erlwanger KH, Rummel C, Roth J, Madziva MT, Harden LM. Brewer’s yeast is a potent inducer of fever, sickness behavior and inflammation within the brain. Brain Behav Immun. 2018;68:211–223. doi:10.1016/j.bbi.2017.10.019
  • Koenig S, Luheshi GN, Wenz T, Gerstberger R, Roth J, Rummel C. Leptin is involved in age-dependent changes in response to systemic inflammation in the rat. Brain Behav Immun. 2014;36:128–138. doi:10.1016/j.bbi.2013.10.019
  • Welsch J, Hubschle T, Murgott J, et al. Fever induction by systemic stimulation with macrophage-activating lipopeptide-2 depends upon TLR2 but not CD36. Innate Immun. 2012;18(3):541–559. doi:10.1177/1753425911426892
  • Peek V, Neumann E, Inoue T, et al. Age-Dependent Changes of Adipokine and Cytokine Secretion From Rat Adipose Tissue by Endogenous and Exogenous Toll-Like Receptor Agonists. Front Immunol. 2020;11:1800. doi:10.3389/fimmu.2020.01800
  • Roth J, McClellan JL, Kluger MJ, Zeisberger E. Attenuation of fever and release of cytokines after repeated injections of lipopolysaccharide in Guinea-pigs. J Physiol. 1994;477(Pt 1):177–185. doi:10.1113/jphysiol.1994.sp020182
  • Voss T, Rummel C, Gerstberger R, Hubschle T, Roth J. Fever and circulating cytokines induced by double-stranded RNA in Guinea pigs: dependence on the route of administration and effects of repeated injections. Acta Physiol. 2006;187(3):379–389. doi:10.1111/j.1748-1716.2006.01587.x
  • Simons CT, Kulchitsky VA, Sugimoto N, Homer LD, Szekely M, Romanovsky AA. Signaling the brain in systemic inflammation: which vagal branch is involved in fever genesis? Am J Physiol. 1998;275(1):R63–68. doi:10.1152/ajpregu.1998.275.1.R63
  • Zeisberger E, Roth J. Tolerance to pyrogens. Ann N Y Acad Sci. 1998;856:116–131. doi:10.1111/j.1749-6632.1998.tb08320.x
  • Savage JC, St-Pierre MK, Hui CW, Tremblay ME. Microglial Ultrastructure in the Hippocampus of a Lipopolysaccharide-Induced Sickness Mouse Model. Front Neurosci. 2019;13:1340. doi:10.3389/fnins.2019.01340
  • Sasaki A, Yasukawa H, Suzuki A, et al. Cytokine-inducible SH2 protein-3 (CIS3/SOCS3) inhibits Janus tyrosine kinase by binding through the N-terminal kinase inhibitory region as well as SH2 domain. Genes Cells. 1999;4(6):339–351. doi:10.1046/j.1365-2443.1999.00263.x
  • Perkins ND. Post-translational modifications regulating the activity and function of the nuclear factor kappa B pathway. Oncogene. 2006;25(51):6717–6730. doi:10.1038/sj.onc.1209937
  • Hayashi Y, Kawaji K, Sun L, et al. Microglial Ca(2+)-activated K(+) channels are possible molecular targets for the analgesic effects of S-ketamine on neuropathic pain. J Neurosci. 2011;31(48):17370–17382. doi:10.1523/JNEUROSCI.4152-11.2011
  • Kaushal V, Koeberle PD, Wang Y, Schlichter LC. The Ca2+-activated K+ channel KCNN4/KCa3.1 contributes to microglia activation and nitric oxide-dependent neurodegeneration. J Neurosci. 2007;27(1):234–244. doi:10.1523/JNEUROSCI.3593-06.2007
  • Hou L, Qu X, Qiu X, Huang R, Zhao X, Wang Q. Integrin CD11b mediates locus coeruleus noradrenergic neurodegeneration in a mouse Parkinson’s disease model. J Neuroinflammation. 2020;17(1):148. doi:10.1186/s12974-020-01823-3
  • Kasumu Adebimpe W, Hougaard C, Rode F, et al. Selective Positive Modulator of Calcium-Activated Potassium Channels Exerts Beneficial Effects in a Mouse Model of Spinocerebellar Ataxia Type 2. Chem Biol. 2012;19(10):1340–1353. doi:10.1016/j.chembiol.2012.07.013
  • Draper CSI. ALS-Induced Excitability Changes in Individual Motorneurons and the Spinal Motorneuron Network in SOD1-G93A Mice at Symptom Onset OhioLINK Electronic Theses and Dissertations Center. Wright State University; 2021.
  • Vichaya EG, Malik S, Sominsky L, Ford BG, Spencer SJ, Dantzer R. Microglia depletion fails to abrogate inflammation-induced sickness in mice and rats. J Neuroinflammation. 2020;17(1):172. doi:10.1186/s12974-020-01832-2
  • Golozoubova V, Cannon B, Nedergaard J. UCP1 is essential for adaptive adrenergic nonshivering thermogenesis. Am J Physiol Endocrinol Metab. 2006;291(2):E350–357. doi:10.1152/ajpendo.00387.2005
  • Nicholls DG, Locke RM. Thermogenic mechanisms in brown fat. Physiol Rev. 1984;64(1):1–64. doi:10.1152/physrev.1984.64.1.1
  • Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J. 2003;374(Pt 1):1–20. doi:10.1042/bj20030407
  • Yarwood SJ, Borland G, Sands WA, Palmer TM. Identification of CCAAT/enhancer-binding proteins as exchange protein activated by cAMP-activated transcription factors that mediate the induction of the SOCS-3 gene. J Biol Chem. 2008;283(11):6843–6853. doi:10.1074/jbc.M710342200
  • Qin H, Yeh WI, De Sarno P, et al. Signal transducer and activator of transcription-3/suppressor of cytokine signaling-3 (STAT3/SOCS3) axis in myeloid cells regulates neuroinflammation. Proc Natl Acad Sci U S A. 2012;109(13):5004–5009. doi:10.1073/pnas.1117218109
  • Dolga AM, Netter MF, Perocchi F, et al. Mitochondrial Small Conductance SK2 Channels Prevent Glutamate-induced Oxytosis and Mitochondrial Dysfunction. J Biol Chem. 2013;288(15):10792–10804. doi:10.1074/jbc.M113.453522
  • Nadjar A, Combe C, Laye S, et al. Nuclear factor kappaB nuclear translocation as a crucial marker of brain response to interleukin-1. A study in rat and interleukin-1 type I deficient mouse. J Neurochem. 2003;87(4):1024–1036. doi:10.1046/j.1471-4159.2003.02097.x
  • Liu DL, Zhao LX, Zhang S, Du JR. Peroxiredoxin 1-mediated activation of TLR4/NF-kappaB pathway contributes to neuroinflammatory injury in intracerebral hemorrhage. Int Immunopharmacol. 2016;41:82–89. doi:10.1016/j.intimp.2016.10.025
  • Srinivasan M, Bayon B, Chopra N, Lahiri DK. Novel Nuclear Factor-KappaB Targeting Peptide Suppresses beta-Amyloid Induced Inflammatory and Apoptotic Responses in Neuronal Cells. PLoS One. 2016;11(10):e0160314. doi:10.1371/journal.pone.0160314
  • Zhang Y, Gao L, Cheng Z, et al. Kukoamine A Prevents Radiation-Induced Neuroinflammation and Preserves Hippocampal Neurogenesis in Rats by Inhibiting Activation of NF-kappaB and AP-1. Neurotox Res. 2016;31(2):259–268. doi:10.1007/s12640-016-9679-4
  • Shakkottai VG, Do Carmo Costa M, Dell’Orco JM, Sankaranarayanan A, Wulff H, Paulson HL. Early changes in cerebellar physiology accompany motor dysfunction in the polyglutamine disease spinocerebellar ataxia type 3. J Neurosci. 2011;31(36):13002–13014. doi:10.1523/JNEUROSCI.2789-11.2011
  • Walter JT, Alvina K, Womack MD, Chevez C, Khodakhah K. Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia. Nat Neurosci. 2006;9(3):389–397. doi:10.1038/nn1648
  • Vick KA, Guidi M, Stackman RW. In vivo pharmacological manipulation of small conductance Ca2+-activated K+ channels influences motor behavior, object memory and fear conditioning. Neuropharmacology. 2010;58(3):650–659. doi:10.1016/j.neuropharm.2009.11.008
  • Lam J, Coleman N, Garing AL, Wulff H. The therapeutic potential of small-conductance KCa2 channels in neurodegenerative and psychiatric diseases. Expert Opin Ther Targets. 2013;17(10):1203–1220. doi:10.1517/14728222.2013.823161
  • Eskilsson A, Mirrasekhian E, Dufour S, Schwaninger M, Engblom D, Blomqvist A. Immune-induced fever is mediated by IL-6 receptors on brain endothelial cells coupled to STAT3-dependent induction of brain endothelial prostaglandin synthesis. J Neurosci. 2014;34(48):15957–15961. doi:10.1523/JNEUROSCI.3520-14.2014
  • Rummel C, Matsumura K, Luheshi GN. Circulating IL-6 contributes to peripheral LPS-induced mPGES-1 expression in the rat brain. Brain Res Bull. 2011;86(5–6):319–325. doi:10.1016/j.brainresbull.2011.09.006
  • Long NC, Vander AJ, Kunkel SL, Kluger MJ. Antiserum against tumor necrosis factor increases stress hyperthermia in rats. Am J Physiol. 1990;258(3 Pt 2):R591–595. doi:10.1152/ajpregu.1990.258.3.R591
  • Koenig S, Bredehoft J, Perniss A, Fuchs F, Roth J, Rummel C. Age Dependent Hypothalamic and Pituitary Responses to Novel Environment Stress or Lipopolysaccharide in Rats. Front Behav Neurosci. 2018;12:55. doi:10.3389/fnbeh.2018.00055
  • Fuchs F, Damm J, Gerstberger R, Roth J, Rummel C. Activation of the inflammatory transcription factor nuclear factor interleukin-6 during inflammatory and psychological stress in the brain. J Neuroinflammation. 2013;10:140. doi:10.1186/1742-2094-10-140
  • Richter M, Nickel C, Apel L, et al. SK channel activation modulates mitochondrial respiration and attenuates neuronal HT-22 cell damage induced by H2O2. Neurochem Int. 2015;81:63–75. doi:10.1016/j.neuint.2014.12.007
  • Richter M, Vidovic N, Honrath B, et al. Activation of SK2 channels preserves ER Ca(2+) homeostasis and protects against ER stress-induced cell death. Cell Death Differ. 2016;23(5):814–827. doi:10.1038/cdd.2015.146
  • Eskilsson A, Shionoya K, Enerback S, Engblom D, Blomqvist A. The generation of immune-induced fever and emotional stress-induced hyperthermia in mice does not involve brown adipose tissue thermogenesis. FASEB J. 2020;34(4):5863–5876. doi:10.1096/fj.201902945R
  • Dittner C, Lindsund E, Cannon B, Nedergaard J. At thermoneutrality, acute thyroxine-induced thermogenesis and pyrexia are independent of UCP1. Mol Metab. 2019;25:20–34. doi:10.1016/j.molmet.2019.05.005
  • Steiner AA, Chakravarty S, Rudaya AY, Herkenham M, Romanovsky AA. Bacterial lipopolysaccharide fever is initiated via Toll-like receptor 4 on hematopoietic cells. Blood. 2006;107(10):4000–4002. doi:10.1182/blood-2005-11-4743
  • Ott D, Murgott J, Rafalzik S, et al. Neurons and glial cells of the rat organum vasculosum laminae terminalis directly respond to lipopolysaccharide and pyrogenic cytokines. Brain Res. 2010;1363:93–106. doi:10.1016/j.brainres.2010.09.083
  • Chakravarty S, Herkenham M. Toll-like receptor 4 on nonhematopoietic cells sustains CNS inflammation during endotoxemia, independent of systemic cytokines. J Neurosci. 2005;25(7):1788–1796. doi:10.1523/JNEUROSCI.4268-04.2005
  • Santos NC, Figueira-Coelho J, Martins-Silva J, Saldanha C. Multidisciplinary utilization of dimethyl sulfoxide: pharmacological, cellular, and molecular aspects. Biochem Pharmacol. 2003;65(7):1035–1041. doi:10.1016/S0006-2952(03)00002-9
  • Hoogland IC, Houbolt C, van Westerloo DJ, van Gool WA, van de Beek D. Systemic inflammation and microglial activation: systematic review of animal experiments. J Neuroinflammation. 2015;12:114. doi:10.1186/s12974-015-0332-6
  • Norden DM, Trojanowski PJ, Villanueva E, Navarro E, Godbout JP. Sequential activation of microglia and astrocyte cytokine expression precedes increased Iba-1 or GFAP immunoreactivity following systemic immune challenge. Glia. 2016;64(2):300–316. doi:10.1002/glia.22930